Reprinted below is the entire series of reports published
during May-July 1963 about a smallpox outbreak in Sweden. Selected
tables and figures from these reports also have been recreated to
resemble the originals as closely as possible. A contemporary

Editorial Note

Sweden -- Stockholm was declared a smallpox infected area on
May 16. A seaman who returned from Indonesia in late March is the
apparent source of an outbreak which has now spread through two
generations of transmission and has resulted in one fatality.
Preliminary information on cases to date, received from the
Ministry of Health, Sweden, and forwarded by Dr. Reimert T.
Ravenholt, Epidemiologic Consultant, Division of Foreign
Quarantine, U.S. Public Health Service, Paris, is given below:

The outbreak was recognized on May 13 when the diagnosis of
smallpox was first suspected in Case #7. The disease was
sufficiently mild in Cases 1, 4, 5 and 12 that medical assistance
was not sought. The only fatality to date occurred in Case #2 who
apparently suffered an acute hemorrhagic form of the disease,
diagnosed as smallpox in retrospect.

This outbreak is of unique interest in that it represents one
of the few epidemics in Western nations in recent years not
evidencing a predominant spread among hospital contacts. Recent
immunization programs among hospital personnel presumably have
altered the pattern of hospital spread observed in other recent
outbreaks. The mildness of the disease in several of the earlier
cases, resulting in the failure of these patients to seek medical
care and hospitalization, has contributed to the pattern of
community transmission.

The outbreak emphasizes the sinister role of mild or
vaccine-modified cases of smallpox in initiating and propagating
outbreaks of severe disease. Since the outbreak was discovered
during the second generation of indigenous cases, it is possible
that Americans recently in Stockholm have been unknowingly exposed
to the disease, and cases of suspicious febrile illness in such
individuals should receive the utmost scrutiny by clinicians and
public health authorities.
{From the May 31, 1963, MMWR}

Four additional cases of smallpox have been identified in
Stockholm with onsets of illness since May 18. All four presumably
acquired their disease as a result of hospital contact.

The outbreak (See MMWR, Vol. 12, page 172) now totals 16
cases, with three generations of transmission following the
importation of smallpox by a seaman who presumably acquired his
disease in transit through Southeast Asia. Information on cases to
date received from Dr. Bo Zetterberg, Chief, Epidemiology Division,
State Bacteriology Laboratory, Stockholm, is summarized in the
table below {See table, page 539} (Table_1).

The pattern of spread of the illness is presented
diagrammatically in the accompanying figure {See figure, page 540}
(Figure_1).

The first case to be identified occurred in an unvaccinated
19-year-old bricklayer (Case 7) who had onset of fever, vomiting,
and backache on May 5. He was hospitalized three days later and
subsequently developed an extensive maculo-papular rash which
became pustular by May 12. Smallpox was suspected and confirmed the
following day by the laboratory.

Immediate epidemiologic investigation revealed that an aunt of
the bricklayer (Case 2) had developed on April 18 an acute febrile
illness, manifest by hemorrhagic skin lesions, and had died shortly
after admission to the hospital on April 23. Ten other cases of
smallpox were identified May 14-16.

The original source of the outbreak was a 24-year-old seaman
who after two weeks residence in Australia left Darwin on March 22
on BOAC Flight #709. In-transit stops of not more than 50 minutes
each were made in Djakarta, Singapore, Rangoon, Calcutta, Karachi,
Teheran, and Damascus en route to Zurich. At Zurich, the seaman
deplaned and the following day boarded Swissair Flight #250,
reaching Stockholm March 24. He apparently acquired his disease as
a result of in-transit exposure either at a terminal or on the
plane. On April 6, 15 days after the flight, he developed a
moderate fever and mild rash and remained in the home of his
grandmother (Case 3) throughout his illness. Cases 2, 3, 4, and 5
all had contact with him in the grandmother's home during the
course of his illness. On April 21, the grandmother fell ill,
subsequently exposing three women (Cases 8-10) who visited the home
to provide nursing care to the elderly woman prior to her
hospitalization on May 27. She was originally diagnosed as having
chickenpox and recovered uneventfully. Another resident of the
building (Case 11) who lived two stories above the grandmother,
developed smallpox but denied acquaintance or contact with the
grandmother.

Case 2, the first fatality, apparently acquired the illness
from the seaman during a visit to the grandmother's apartment and
subsequently transmitted it to her husband (Case 6) and her nephew
(Case 7) the first identified case. Case 12 who had only fever and
serologic evidence of infection, acquired his disease presumably
from his fiancee, Case 4.

The appearance of cases among hospital contacts is more
consistent with the previously observed patterns of imported
smallpox in Western countries. Case 13 is a gardener at the
Infectious Disease Hospital where Cases 3 and 6 were admitted as
presumptive chickenpox on April 27 and May 7, respectively. He is
thought to have handled laundry from these patients prior to the
first suspicion of smallpox on May 12. He was initially employed by
the hospital only two months previous and had not yet been
vaccinated in the hospital's annual revaccination program.

Case 14 was a patient admitted to the Infectious Disease
Hospital with whooping cough on April 30. She was located in the
same hospital vicinity as Case 6, although there was no connection
between the rooms housing these patients. Cases 15 and 16 were
patients on the same hospital ward to which Case 9 was admitted on
May 9. Case 9 was originally thought to have a toxic drug eruption
prior to her diagnosis of smallpox on May 15.

With the exception of Case 12 who had an exceptionally mild
illness, it is apparent that spread of the disease to date has been
primarily among individuals vaccinated at times far distant in the
past. Of the three fatalities to date, one occurred in a person
never vaccinated and the other two in persons vaccinated more than
50 years prior to exposure. The absence of additional spread to
hospital personnel is probably related to efforts in Sweden to
emphasize revaccination of hospital personnel at frequent
intervals. Notably, the last four cases have occurred in persons
already identified and isolated by virtue of being known contacts.

Some 8,000 persons living in neighborhoods of the earlier
cases have been vaccinated. In addition, vaccination has been
provided for other residents of Stockholm on request and to date
some 300,000 persons have availed themselves of this protection.
{From the June 7, 1963, MMWR}

Three additional cases, two hospital acquired, were identified
last week bringing to 19 the total number of smallpox cases
comprising the current outbreak, according to information made
available by Dr. Bo Zetterberg, Chief, Epidemiology Division, State
Bacteriology Laboratory, Stockholm.

Two of the three cases are actually part of the second
generation of transmission (See MMWR Vol. 12, pg. 174), having now
been identified retrospectively by serologic means. Neither patient
developed a rash. Both were nurses in the Stockholm Infectious
Disease Hospital in close contact with the smallpox cases admitted
there. The first, a 44-year-old female, cared for Case No. 3 from
April 27 to May 7 daily, including bathing and local treatment of
the lesions. On May 9, the nurse developed fever and headache, as
well as nausea and low back pain. Except for May 13 and 14, she
continued to work throughout her illness until isolated on May 18.
She was found to have a very high hemagglutination inhibition
antibody titer suggesting recent infection. Her last vaccination
prior to onset of illness was in 1962. She was also in daily
contact with Cases 6 and 14, and directly or indirectly may have
transmitted the disease to Case 14.

The second nurse, a 22-year-old female, also employed in the
Stockholm Infectious Disease Hospital, had daily contact with Case
No. 2 during the period April 27-May 7. On May 11, she experienced
onset of headache, fever, and sore throat and was absent from work
May 11 through May 13. No rash developed. A high HAI titer verified
the diagnosis of smallpox. She had previously been vaccinated in
1950 but at the time of exposure had not yet been revaccinated
under the hospital's annual revaccination program.

The final additional case is that of a 47-year-old man who had
onset of illness May 21 while already isolated as a contact. He is
the father of Case 7, the first identified case. He had never been
vaccinated until 7 days before onset of illness.

The total number of hospital-acquired cases now stands at 6,
one-third of the secondary indigenous cases. The evidence supports
close contact as the primary requisite for spread both in the
hospital and in the community. The disease has spread among persons
vaccinated more than 7 years prior to the time of their exposure
with 2 notable exceptions, both patients with mild disease without
rash. The table below presents data on the vaccination status of
the 18 indigenous cases {See table below} (Table_2).
{From the June 14, 1963, MMWR}

Two additional cases of smallpox were identified in Stockholm
last week bringing to 21 the total number of cases in the current
outbreak. Unique circumstances involving these two persons, neither
of whom were under surveillance as contacts at the time of their
detection, indicates that the outbreak may perhaps be expected to
continue.

Information made available by Dr. Bo Zetterberg, Chief,
Epidemiology Division, State Bacteriology Laboratory, Stockholm,
indicates that on June 6 an 85-year-old woman, who lives with her
daughter, went to a hospital out-patient department for routine
follow-up of a chronic medical problem. The daughter called in
advance informing clinic personnel that the elderly woman had
developed a rash. On arrival at the out-patient clinic, the mother
spent some time in the general waiting room and was then referred
to the dermatology clinic, and again spent some time in the
dermatology waiting room. When seen by physicians, a clinical
diagnosis of smallpox was made. In all, she had spent some four
hours at the hospital and presumably exposed some 450 persons in
the two crowded waiting rooms. It was noted that on May 28 she had
developed a low-grade fever with dizziness, followed by the
appearance of rash on June 2.

She and her 54-year-old daughter share an apartment in a
boarding house for women housing some 100 occupants. The daughter
works as a mortician and on April 26 had prepared the body of
smallpox Case 2 of the outbreak for cremation. She had been placed
under surveillance as a contact and 16 days after her exposure to
the dead woman, having had no symptoms or signs of illness, she was
released from quarantine. She denied any evidence of illness since
being released from surveillance. The total elapsed time from her
contact with the body of Case 2 and the onset of disease in her
mother was 32 days, consistent with two incubation periods of
smallpox. Except for the daughter's exposure, no epidemiologic
evidence could be found linking the mother with a source of
smallpox. Neither the mother nor daughter had been vaccinated since
childhood. The daughter demonstrated a high HAI titer on June 6,
suggesting a recent infection, and in the absence of an alternative
explanation, it may be presumed that the daughter developed a
sub-clinical infection and transmitted virus to her mother. Two
very unusual aspects of smallpox transmission seem apparent. The
daughter, unvaccinated since childhood and exposed to hemorrhagic
smallpox, developed an infection so mild as to produce no symptoms,
yet developed serologic evidence of infection. Despite the presumed
absence of any rash or systemic manifestations of disease, she was
apparently able to transmit the illness to her mother.

The inadvertent exposure of the mother during her eruptive
stage to some 450 persons at the hospital, as well as possible
contacts in the boarding house, establishes an additional large
group of contacts in which cases may yet occur.

An epidemic curve for the outbreak to date is presented
showing the chronologic relationship of the generations of
transmission {See Figure below} (Figure_2). Using the median
date
in the span of onset dates for each generation, it is apparent that
the median incubation periods for all generations are strikingly
similar. {From the July 3, 1963, MMWR}

No new cases have been reported during the past week. The
total number of confirmed cases remains at 23, including four
deaths. The fourth death reported involved an unvaccinated
47-year-old male who died on June 15, 25 days after onset of
illness. He was the father of case 7, also a fatality (See MMWR,
Vol. 12, No. 21, pp. 174 and 183).
{From the July 19, 1963, MMWR}

Two additional cases of smallpox were reported from Stockholm
on July 11 and July 12, respectively. One of these, an 89-year-old
female patient in a mental hospital, had onset of rash and fever on
July 7, 15 days after onset of illness in Case 23, a 73-year-old
woman also hospitalized at this institution.

The total number of confirmed cases that has occurred during
the outbreak is 25, including four deaths.

Editorial Note -- 1996: Reading this MMWR account of the outbreak
of
imported smallpox in Sweden during April-July 1963 is as haunting
now as it was frightening then. At the time, there was justifiable
concern about possible spread of infection from Sweden to the
United States, and when residents of Stockholm were offered
vaccination during the outbreak, "some 300,000 persons...availed
themselves of this protection."

Sweden was the first major country to eliminate indigenous
smallpox, a distinction it achieved in 1895 (1). This outbreak was
the first appearance of imported smallpox there since 1932, except
for a single case in 1945 (2). Infecting 25 persons over six
indigenous generations of transmission, this was one of the larger
such outbreaks in Europe (which had two other imported outbreaks in
1963, four in 1962, and 10 in 1961, for example) after 1958 (3).
Despite Sweden's active vaccination efforts among hospital
personnel, eight of the indigenous cases were acquired by hospital
staff or patients; most of the remainder were infected by
face-to-face contact in the homes of case-patients. However, the
versatile virus apparently also spread in this one outbreak from a
corpse, from laundry of another case-patient, and by remote
airborne exposure, and its clinical presentation ranged from six
cases (among persons with old vaccinations) who did not develop a
rash at all to at least one hemorrhagic case.

Several aspects of the outbreak in Sweden differed
dramatically from smallpox outbreaks in Great Britain the previous
winter following importations from Pakistan. In particular, this
outbreak was not recognized until seven cases already had occurred;
ambulatory cases with "mild" disease were important in early
transmission; the overall case-fatality rate was substantially
lower (15% in Sweden versus 40% in Great Britain). At the time,
these differences were attributed to vaccine-modification of
smallpox associated with the ameliorating influence of partial
immunity from distant prior vaccinations. In retrospect, they may
reflect infection with a strain of smallpox virus from Indonesia
where smallpox historically seemed to be less lethal than on the
Indo-Pakistan subcontinent.

In the outbreak in Sweden, hospital transmission of smallpox
was not prominent in the early generations of disease as it was in
most other European outbreaks associated with importation. However,
once patients began to be admitted to the hospital, the hospital
became the focus of transmission. In addition, transmission also
was associated with contact with fatal cases; indeed, handling
smallpox corpses and attending funerals of smallpox victims
resulted in outbreaks in Africa and other smallpox-endemic areas
during the global smallpox eradication campaign (4).

Dr. Ronald R. Roberto, an officer in CDC's Epidemic
Intelligence Service Program during 1962-1964, went to Stockholm as
an international observer during this outbreak. In addition to his
role in rapidly communicating emerging information to CDC, he
formed relationships with Swedish colleagues -- including
epidemiologists H. B. Lundbeck and B. O. Ringertz and virologist J.

Espmark -- who made important contributions to the subsequent
development of smallpox eradication activities of CDC and the World
Health Organization.

This outbreak also highlights how interconnected the world was
already in 1963, and it illustrates vividly the potential danger
posed to all other humans as long as smallpox existed anywhere on
the planet. Even discounting the unknown, apparently chance
encounter by which the index patient in this outbreak came to be
infected, the capricious nature of many of the subsequent
encounters that resulted in indigenous cases in Sweden is
breathtaking. The painful lesson was not lost on Sweden, which
contributed almost $16 million to the global Smallpox Eradication
Program, beginning in 1967, making it the second largest donor
after the United States (3). Sweden's generosity was especially
important during the final battles against smallpox in India,
Bangladesh, and Somalia.

Finally, it is fitting that CDC marks the 50th Anniversary of
its own founding by commemorating the 200 years since Edward Jenner
discovered vaccination in May 1796 and the 30 years since the
Nineteenth World Health Assembly resolved in May 1966 to eradicate
smallpox over the next 10 years. The CDC effort in helping 20 West
and Central African countries to eradicate smallpox early in the
global campaign with support provided by the U.S. Agency for
International Development and by the Public Health Service remains
one of its finest and most beneficial achievements.

The glorious legacy of the global Smallpox Eradication Program
lives today in the campaigns to eradicate dracunculiasis and
poliomyelitis. Others too will follow.

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